Intraspecies variation in dominance style of Macaca fuscata

Knowledge of intraspecific variation is important to test the evolutionary basis of covariation in primate social systems, yet few reports have focused on it, even in the best-studied species of the Macaca genus. We conducted a comparative study of the dominance styles among three provisioned, free-ranging groups of Japanese macaques at Shodoshima Island, Takasakiyama Mountain and Shiga Heights, and collected standard data on aggressive and affiliative behavior during a period of 5 years. Our data in the Takasakiyama and Shiga groups support previous studies showing that Japanese macaques typically have despotic social relations; nevertheless, our data in the Shodoshima group are inconsistent with the norm. The social traits of Shodoshima monkeys suggested that: (1) their dominance style is neither despotic nor tolerant but is intermediate between the two traits; (2) some measures of dominance style, e.g., frequency and duration of social interactions, covary as a set of tolerant traits in Shodoshima monkeys. This study suggests broad intraspecific variation of dominance style in Japanese macaques as can be seen in some other primate species.     

Genetic variation of the cytoplasmic and mitochondrial malic enzymes in the monkey Macaca nemestrina

Electrophoretic variation of both the cytoplasmic and mitochondrial forms of the malic enzyme is described in Macaca nemestrina. Pedigree analysis of the observed phenotypes demonstrates that the two subcellular forms of the malic enzyme are genetically independent. The identity of the electrophoretic phenotypes in brain, heart muscle, liver, kidney, adrenal, and spleen from any given individual shows that each subcellular form is determined by the same genetic locus in a wide variety of tissues. After separation by ion exchange chromatography, the cytoplasmic and mitochondrial malic enzymes were shown to be distinct in their heat stability and K_m for malate, but no significant differences were found among the variants of the cytoplasmic enzyme or among the variants of the mitochondrial enzyme. It is possible that the polymorphism of the mitochondrial malic enzyme is selectively neutral.This study was supported by grant GM-15253 from the National Institutes of Health. One of us (G.S.O.) was a Special Fellow, U.S. Public Health Service (5F3 HD 43, 122-02); Fellow, National Genetics Foundation.     

Genetic variation in transferrin alleles of rhesus macaques, Macaca mulatta

The rhesus macaque displays an extensive polymorphism at the transferrin locus. A principal components analysis describes the variance and covariance of alleles at the transferrin locus in eight widely dispersed sample populations. Using an eigenvectorial representation of the covariance matrix and systematically approximated geographical locations the distribution of populations and transferrin alleles is compared. Alleles with high variance prove to be the determining factor in the placement of populations in a "genetic map" and provide a means for interpreting the low congruence of genetics and geography found.     

Craniodental variation among Macaques (Macaca), nonhuman primates

Background  

In terms of structure and function, the skull is one of the most complicated organs in the body. It is also one of the most important parts in terms of developmental and evolutionary origins. This complexity makes it difficult to obtain evolutionary assessments if, as is usually the case with fossils, only part of the skull is available. For this reason this study involves a set of comparisons whereby the smallest functional units are studied first, and these built up, through a triple-nested hierarchical design, into more complex anatomical regions and eventually into the skull-as-a-whole. This design has been applied to macaques (Macaca) in order to reveal patterns of variation at the different levels. The profiles of such variation have been obtained both within and between species. This has lead to a search for the skull parts that have undergone similar selection pressures during evolution and comparable development patterns in both ontogeny and phylogeny.     

Intraspecific red cell enzyme variation in the pigtailed macaque (Macaca nemestrina)

The erythrocytes of 350 pigtailed macaques (Macaca nemestrina) were examined for electrophoretic variation of hemoglobin and 26 enzymes. Seven enzymes showed variation in more than 1% of individuals: phosphoglucose isomerase, phosphoglucomutase-1, soluble NADP-dependent isocitric dehydrogenase, peptidase A, peptidase C, 2,3-diphosphoglycerate mutase, and acid phosphatase. Variation with lesser frequency was found in soluble glutamic-oxalacetic transaminase, phosphoglycerate kinase, lactic dehydrogenase, and hemoglobin. Only eight samples were tested for esterase D, and one of these had a variant phenotype. Enzymes with no clear variation were adenylate kinase, adenosine deaminase, phosphofructokinase, hexokinase, pyruvate kinase, glyceraldehyde 3-phosphate dehydrogenase, aldolase, phosphoglycerate mutase, phosphopyruvate hydratase (enolase), phosphoglucomutase-3, and superoxide dismutase. There was father-to-son transmission of PGI, PGM-1, peptidase C, 6PGD, 2,3-DPGAM, NADP-ICD, and acid phosphatase variants, suggesting that these loci are autosomal as in man.     

Expression of nerve growth factor and its receptors in the somatosensory-motor cortex of Macaca nemestrina

The present study was designed to examine the nerve growth factor (NGF) system (ligand and receptor-expressing neurons) in the somatosensory (areas 1, 3a, and 3b) and motor (area 4) cortices of the mature macaque. Light and electron microscope immunohistochemistry was used to assess the distribution and identity of NGF-, p75-, and trk-expressing elements. In each cortical area examined, NGF-positive neuronal somata were distributed through all laminae; most immunolabeled neurons were in layers II, III, and V. Based upon light microscope criteria (e.g., the morphology of proximal dendrites), both pyramidal and stellate neurons expressed NGF. Of the identifiable NGF- immunoreactive cells, 92% were pyramidal neurons and the remainder was stellate neurons. The electron microscope study showed that most (88%) NGF-positive somata formed symmetric synapses, whereas the others formed both symmetric and asymmetric synapses. As the somata of pyramidal neurons form only symmetric synapses and those of inhibitory stellate neurons form both symmetric and asymmetric somatic synapses, the ultrastructural data support the light microscopic analyses. In contrast, neurotrophin receptors, p75 and trk, were expressed chiefly by the cell bodies of layer V pyramidal neurons and the supragranular neuropil. At the ultrastructural level, receptor-positive profiles were post-synaptic elements (e.g., dendritic shafts and spines) and the concentration of immunoreactivity was greatest in the vicinity of post-synaptic densities. Thus, NGF regulatory systems parallel excitatory and inhibitory neurotransmitter systems. Cortex contains the morphological framework by which pyramidal and/or inhibitory stellate neurons can affect the activity of post-synaptic pyramidal neurons via anterograde and autocrine/paracrine NGF systems.     

Retrograde degeneration of the pyramidal cells in the motor cortex of apes (Macaca fascicularis)]

In three adult macaques the retrograde degeneration of cell bodies in the motor cortex was investigated 6 months after unilateral pyramidal tract section. Large and small Betz cells of the fifth layer were identified microscopically and counted. The analysis of the data reveals that after pyramidotomy, (1) contrary to our expectations from the extent of the pyramidal lesions, a surprising percentage of undegenerated Betz cells remains in the contralateral motor cortex, (2) a greater percentage of small rather than large cell survives, and (3) the greatest loss of cells is in the foot region, the smallest in the face region. The results are discussed in relation to the role of pyramidal axon collaterals in the survival of cell bodies, and the distinction between pyramidal cells and pyramidal tract cells.     

Microsatellite variation in two subspecies of cynomolgus monkeys (Macaca fascicularis)

To estimate the genetic variability of two subspecies of cynomolgus monkeys (Macaca fascicularis fascicularis and M. f. aurea) using microsatellite markers, 26 microsatellite markers were selected from previous reports. Seventeen markers showed high polymorphism in a subset of monkeys and were used for the assessment of genetic diversity in the larger sample. The effective number of alleles, the polymorphism information content (PIC) and the expected heterozygosity of M. f. aurea monkeys were all statistically significantly higher than those of M. f. fascicularis monkeys (P < 0.05), suggesting the M. f. aurea monkeys had a higher degree of genetic variation than the M. f. fascicularis monkeys. Substantial differences in allele distribution were also detected between the two subspecies of cynomolgus monkeys. Private alleles restricted to the M. f. fascicularis or the M. f. aurea monkeys were found throughout the selected 17 loci. These private alleles may allow the discrimination of the two subspecies of cynomolgus monkeys. The selected markers could also be used to estimate the genetic variation for other subspecies of cynomolgus monkeys. Further work using additional animals obtained from native or independent sources will be important for a more complete understanding of the genetic differences between these two subgroups.     

Seasonal variation of reproductive parameters in the laboratory-housed male cynomologus macaque (Macaca fascicularis).

Changes in body weight, sperm concentration and testicular volume were monitored for a 13-lunar month period in seven laboratory-housed adult male Macaca fascicularis. No significant change was noted in body weight or sperm concentration between periods of maximal and minimal mean values nor between periods standardized for comparison between the three parameters. Testis volumes were significantly greater during the months of July through early September and during the standardized period of May through July than during January through March and the standardized interval October through January.     

Differentiation of neural cells in the fetal cerebral cortex of cynomolgus monkeys (Macaca fascicularis)

Proliferation and programmed cell death are important in the formation of morphologic structures and functional activity during CNS development. We used immunohistochemical and TUNEL methods to examine the proliferation and differentiation of neural cells in, distribution of apoptotic cells in, and microglial cell involvement in the removal of apoptotic cells from the fetal cerebral cortex of cynomolgus monkeys. At embryonic day (E) 50 and E80, the neuroepithelium contained many mitotic cells. Cells staining for PCNA (a nuclear marker of proliferating cells) were prominent in the proliferative zone, whereas cells positive for NeuN (a neuron-specific marker) were absent. GFAP staining for glial cells was positive in the neuroepithelium and radial glial fibers. Iba1-positive cells (that is, macrophages and microglia) were distributed throughout all regions at all time points but accumulated especially in the ventricular zone at E80. Apoptotic morphology (at E80) and TUNEL-positive cells (that is, containing DNA fragmentation; at E50 and E80) were observed also. At E120 and E150, most PCNA-positive cells were in the ventricular zone, and NeuN-positive cells were prominent in all layers except layer I-II at E120. GFAP immunoreactivity was detected mainly in cells with fine processes in the white matter. Neither apoptosis nor TUNEL-positive cells were detected at either E120 or E150. These results suggest that proliferation, migration, and neural cell death occur during midgestation (that is, E50 to E80) in fetal brain of cynomolgus macaques, whereas differentiation and maturation of neural cells occur after midgestation (E80).     

Effects of geographic origin on captive Macaca mulatta mitochondrial DNA variation

Partial sequences from mitochondrial (mt) 12S and 16S rRNA genes were analyzed to characterize diversity among captive rhesus macaques (Macaca mulatta) originating from various geographic regions. Several nested clades, defined by closely related haplotypes, were identified, suggesting considerable genetic subdivision, probably relics from heterogeneous origins, founder effects, and genetic drift, followed by breeding isolation. The rhesus matrilineages from India differed discretely and markedly from Chinese matrilineages; approximately 90% of the genetic heterogeneity among the combined samples of Indian and Chinese rhesus macaques studied here was due to country of origin. In addition, mtDNA sequences from macaques of China were more diverse than those from rhesus macaques of India, an outcome consistent with China's greater subspecies diversity and with nuclear genotype distributions. Otherwise, the distribution of mtDNA variation within rhesus macaques of China, and especially within those of India, exhibited far less structure and did not conform to a simple isolation-by-distance model. As the demand for genetically heterogeneous and well-characterized rhesus macaques for biomedical-based research increases, mtDNA haplotypes can be useful for genetically defining, preserving maximal levels of genetic diversity within, and confirming the geographic origin of captive breeding groups of rhesus macaques.     

Social behavior in stump-tailed macaques (Macaca speciosa) after lesions of the dorsolateral frontal cortex

This experiment observed the effects of dorsolateral frontal cortex ablations on quantified social interactions of stump-tail macaques within the context of the social behavior of a larger group. A caged group of 11 stump-tail macaques, six females and five males, was observed for 100 hours pre-operatively. Post-operatively, five operates and five sham operates matched for sex, age, and rank were observed for 110 hours. Aggression increased following surgery. The female operates ranked No. 3 and No. 5 were seen to fall to the bottom of the dominance hierarchy two months after surgery. The fall in dominance as measured by displacement behavior was found to permeate several behavioral categories including presenting, threatening, and aggression. The female operates appeared to fall in inverse relationship to their ranks. The male operates showed minimal disruptions after surgery. The length of the time between surgery and the outbreak of violence might represent the length of time required for subordinates to notice and confirm the behaviors resulting from attentional defects in the high-ranking female operates.     

Quantitative genetic variation in carbonic anhydrase isozymes from tissues of the pig-tailed macaque,Macaca nemestrina

Two isozymes of carbonic anhydrase (CA I and CA II) were quantified by a radio-immunoassay in 10 different tissues of the pig-tailed macaque. There were clearly differences in relative amounts of the two isozymes, indicating a differential regulation of these two different gene products. An inherited deficiency variant reduced red cell CA I and CA II 5000-fold and 2.7-fold, respectively. In nine other tissues, CA I was reduced from approximately twofold to 110-fold, and CA II was essentially unchanged. The CA I in deficient red cells was immunochemically and electrophoretically identical to common electrophoretic variants of CA I in the pig-tailed macaque and was enzymatically active.This work was part of a doctoral dissertation submitted in partial fulfillment of the Doctor of Philosophy degree in the Horace H. Rackham School of Graduate Studies at The University of Michigan. Supported by NIH training grant 5-T01-GM-71-11 and NIH research grant GM-15419.     

Sources of variation in interbirth intervals among captive bonnet macaques (Macaca radiata)

Female fitness is a function of variation in the length of females' reproductive careers, the viability of their offspring, and the frequency with which they give birth. Infant loss shortens interbirth intervals in most primate species, but we know considerably less about other factors that contribute to variation in the length of interbirth intervals within groups. In one large captive group of bonnet macaques, maternal parity, age, experience, family size, and recent reproductive history are all associated with variation in the length of intervals that follow the birth of surviving infants. Primiparous females have the longest interbirth intervals, while multiparous females who have produced surviving infants in the past and have raised their last infant successfully have the shortest interbirth intervals. Infant sex and maternal rank have no direct effect upon the length of interbirth intervals. One of the underlying causes of variation in the length of interbirth intervals after surviving births seems to be variation in the timing of conceptions among females. Females who conceive early in the mating season tend to have shorter interbirth intervals than other females. However, females who are multiparous, experienced, and have recently raised infants have late conceptions and short interbirth intervals.     

Species variation in the localisation of esterases in the cerebellar cortex of mouse and bat

A comparative study of the distribution of a simple esterase and acetylcholinesterase in the cerebellar cortex of mouse and bat has been made. The Purkinje layer is intensely positive for simple esterase in both species. The granular and molecular layers showed mild to moderate activity in mouse and intense activity in bat. Acetylcholinesterase in cerebellar layers of bat is more intense than in mouse. In bat cerebellum, acetylcholinesterase is observed in the dendrites of Purkinje cells, but not in their cell bodies. Acetylcholinesterase was not found in Purkinje cells of mouse.     

Ultrastructural analysis of major basement membrane types in rhesus monkey Macaca mulatta acellular renal cortex

Increasing interest in animal models of human nephropathies have led to a number of renal studies in nonhuman primates. In the current investigation, sequential detergent extraction of cellular elements was carried out on renal cortical tissue blocks from rhesus monkey in an effort to demonstrate clearly the morphological features of major basement membrane (BM) types and their associated extracellular matrix (ECM). LM and TEM views of acellular tissue blocks demonstrate planar arrangements of ECM components, while SEM studies provide striking three-dimensional images of their surface characteristics. All major BM types maintain their in vivo histoarchitectures despite the absence of cells. We propose that the intrinsic structural rigidity of tubular (TBM), Bowman's capsule (BCBM) and peritubular capillary BM (PTCBM) may be related to to their close external association with collagenous fibrils, while glomerular BM (GBM) may be internally supported by a network of mesangial matrix (MM) plates and trabeculae which extend onto internal surfaces of peripheral GBM loops. Thicknesses of rhesus monkey renal BMs show that they are similar to those seen in the laboratory rat and, in general, BCBM greater than TBM greater than GBM greater than PTCBM. We conclude that rhesus monkey renal BMs closely resemble those described by us in the human [J. Ultrastruct. Res. 82: 96-110, 1983] and that this species offers an attractive model for studies of renal diseases of BM origin-notably diabetes mellitus.     

Characteristics of the menstrual cycle in nonhuman primates. I. Similarities and dissimilarities between Macaca fascicularis and Macaca arctoides.

Comparative studies of reproductive characteristics were carried out on a colony of Macaca fascicularis and M. arctoides. Seasonal differences were not significant between species, and conceptions occurred throughout the year. The occurrence of short cycles ('luteal phase defect') was found in 2.9% of all M. fascicularis cycles and 1.5% of all M. arctoides cycles. Long cycles (40-50 days) were found in 4.0% of all M. fascicularis cycles and 3.5% of all M. arctoides cycles. Gestation lengths averaged 172.4 and 165.3 days, respectively, for M. arctoides and M. fascicularis. Ovulation in M. fascicularis occurred at a day of ovulation/cycle length ratio of 0.48 +/- 0.08 compared with 0.48 +/- 0.09 for M. mulatta data previously published.